Figure 3.7 Discontinuous gas exchange cycles in Omorgus radula (Coleoptera, Trogidae) recorded at 24°C.

Source: Bosch et al. (2000). Physiological Entomology 25, 309-314, Blackwell Publishing.

Ventilation at rest

In those species where active ventilation accompanies gas exchange at rest, ventilatory movements can include active abdominal pumping (by means of dorso-ventral and telescoping movements), head protraction and retraction, and prothoracic pumping (Miller 1981; Harrison 1997). The proportion of tracheal air estimated to be exchanged with each stroke is in the region of 5-20 per cent for Schistocerca gregaria (Orthoptera, Acrididae), although some recent estimates (Westneat et al. 2003), have suggested a much higher value for other insects. Although some small insects, such as ants, appear not to use ventilation for gas exchange (Lighton 1996), others ventilate vigorously (Miller 1981).

Time (min)

Figure 3.8 Cyclic gas exchange in pseudergate of Incisitermes tabogae (Isoptera, Kalotermitidae).

Time (min)

Figure 3.8 Cyclic gas exchange in pseudergate of Incisitermes tabogae (Isoptera, Kalotermitidae).

Source: Comparative Biochemistry and Physiology A, 129, Shelton and Appel, 681-693, © 2001, with permission from Elsevier.

Haemolymph circulation also plays a considerable role in tracheal ventilation, especially in adult insects. This is largely as a consequence of the presence of many large air sacs and the compartmental-ization of the haemocoel into an anterior section comprising largely the thorax and often the first abdominal segment, and a posterior section, consisting of the abdominal segments (Wasserthal 1996; Hertel and Pass 2002). This compartment-alization is especially distinct in the aculeate Hymenoptera owing to their petiole, the narrow segment that separates the first abdominal segment from the remainder of the abdomen. In flies such as Calliphora, haemolymph flow reversal, associated with heartbeat reversal, interacts with the air sacs to produce inspiration via the abdominal spiracles during forward heartbeat, and collapse of the abdominal air sac and expiration via the abdominal spiracles during retrograde heartbeat (Fig. 3.9). Similar interactions between circulation and ventilation have been documented in many other adult insects (see review for the holometabolous insects provided by Wasserthal 1996). In bumblebees, moths, and beetles these interactions are important for thermoregulation (Chapter 6). Accessory pulsatile organs also play a significant role in circulation (insects have more 'hearts' than most other organisms), and the interaction between circulation and gas exchange (Hertel and Pass 2002).

In several insect species, extracardiac pulsations associated with contraction of abdominal, intersegmental muscles are thought to be important for gas exchange as a consequence of their

Figure 3.9 Gas exchange dynamics in Calliphora vicina (Diptera, Calliphoridae) resulting from haemolymph oscillation between the anterior and posterior body.

Source: Reprinted from Advances in Insect Physiology, 26, Wasserthal, 297-351, © 1996, with permission from Elsevier.

pronounced effect on haemocoelic pressure (Sláma 1988, 1999). Although heartbeat reversal (cardiac pulsation) is an important contributor to gas exchange in lepidopteran pupae (Hetz et al. 1999), and abdominal movements are likewise important for gas exchange in some beetle species (Tartes et al. 2002), the significance of extracardiac pulsations remains moot. While Slama (1994, 1999) has vigorously defended both the importance of extracardiac pulsations and the significance of the coelopulse system for regulation of respiration, it appears that they play only a minor role in gas exchange and the regulation of respiration, respectively (Lighton 1994; Wasserthal 1996; Tartes et al. 2002).

Ventilatory movements are largely controlled by the central nervous system (CNS) via the action of the abdominal ganglia and a central pacemaker located in the fused abdominal or metathoracic ganglia, or in abdominal ganglia (Ramirez and Pearson 1989), as well as by afferent feedback from abdominal ganglia and proprioceptors. Manipulations of pO2 and pCO2 have a pronounced effect on ventilation rate (Miller 1981), suggesting that there is central chemoreception of oxygen and carbon dioxide in the CNS (Miller 1974; Harrison 1997). Recently, Bustami et al. (2002) provided the first clear evidence for such central chemoreception, showing similar ventilatory responses to changes in pO2 and pCO2 of both the CNS in vitro and whole animals. Moreover, they also demonstrated a biphasic response to hypoxia, characterized by an initial extreme increase in ventilation rate, followed by complete cessation of activity, and argued that such a response, which is more typical of vertebrates, provides an indication that ventilatory networks across the animal kingdom share many basic functions. Other experimental work on grasshoppers such as Romalea guttata and Schistocerca americana has demonstrated that in alert, but quiescent individuals, manipulation of endotracheal pO2 and pCO2 has pronounced effects on abdominal pumping rate, as might be expected (Gulinson and Harrison 1996). However, changes in pH have little effect on abdominal pumping rates (except through pCO2 changes associated with injection of HCO3). Indeed, it appears that in grasshoppers and possibly in other insects, the ventilatory system participates indirectly in acid-base regulation by maintaining a relatively constant tracheal pCO2, while the excretory system (gut and Malpighian tubules) is responsible for responding to pH changes and for regulating non-volatile acid-base equivalents (Gulinson and Harrison 1996; Harrison 2001).

Spiracular control

Gas exchange pattern and efficacy are markedly affected by the degree of synchronization between the spiracles and abdominal pumping (Miller 1973). In many insects there is close central coordination of spiracular and ventilatory movements (Harrison 1997), which often results in unidirectional, retrograde airflow at rest. As is the case with ventilatory movements, spiracular opening and closing are affected by both pO2 and pCO2, although their effects depend both on the type (single closer muscle, or opener and closer muscles) and location of the spiracles, and vary between species. Generally, the effect of pO2 on spiracular control is mediated via the CNS, whereas carbon dioxide can have either a direct, local effect on the spiracles, or both a direct influence on the spiracles and an effect via the CNS (Miller 1974; Kaars 1981). In some mantids and cockroaches, for example, CO2 first has a local effect, causing the spiracular valve to open, and later reaches the CNS, which then has a direct effect on the muscle, allowing further spiracular opening.

Spiracular movements are also affected by the hydration state of the organism and the humidity of the surrounding environment. In various dragonfly species, partial dehydration causes an increase in the threshold of spiracular responses to CO2 and O2. Miller (1964) suggested that increases in concentration of certain ions, rather than osmotic pressure overall, are responsible for the change in spiracular control. A similar increase in spiracular control can be found in partially dehydrated tsetse flies (Bursell 1957), and in Aedes sp. (Diptera, Culicidae) the spiracles are responsive to the relative humidity of outside air (Krafsur 1971). Other factors affecting spiracular control include injury, starvation, and temperature (Section 3.4.2), while pH has little effect either directly or via the CNS.

Although spiracular control is often synchronized with ventilatory movements to produce a unidirectional airflow, there is much variation in the degree of spiracular coordination, ventilatory movements, and airflow, among species, among individuals, and even within individuals. Thus, gas exchange may take place through either one or all of the spiracles, spiracular coordination can either be tightly regulated or completely unsyn-chronized, and airflow may be unidirectional (in either direction and reversible), tidal, or in the form of cross-currents (Buck 1962; Kaars 1981; Miller 1981; Slama 1988). In flightless beetles, it has long been maintained that airflow is unidirectional, from the thoracic spiracles to the abdominal spiracles, thus ensuring expiration into a subelytral chamber that would restrict water loss (Hadley 1994a,b). However, investigations of a large, flightless scarab beetle, Circellium bacchus, have raised doubts concerning this conventional interpretation of the role of the subelytral chamber in beetle water economy (Duncan and Byrne 2002; Byrne and Duncan 2003). Rather than being characterized by retrograde airflow at rest, airflow in this species is either tidal or anteriograde, with a clear division of labour between the thoracic and abdominal spiracles, and the entire respiratory demand often being served by a single mesothoracic spiracle. A similar division of labour between the thoracic and abdominal spiracles has been found in the desert-dwelling ant Cataglyphis bicolor (Lighton et al. 1993a), and might reflect a means of restricting water loss in insects, particularly because the abdominal spiracles are generally small and play an important role in oxygen uptake.

A large proportion of the variation in gas exchange patterns within and among individuals is clearly a function of external factors (e.g. temperature, water availability) or the physiological status of the individual (e.g. levels of dehydration, starvation, or activity) (Lighton and Lovegrove 1990; Quinlan and Hadley 1993; Chappell and Rogowitz 2000). However, insects at rest also show much variability in gas exchange patterns that cannot be ascribed to these factors. For example, Miller (1973, 1981) reported considerable among- and within-individual variation in ventilatory patterns of Blaberus sp. (Blattaria, Blaberidae), although he thought that at least some of this variability might have been due to activity of the insects. In the case of lepidopteran pupae, movement is unlikely to be a major source of variation, yet, in some species the pupae show substantial variation in gas exchange patterns both within and between individuals of the same age. Recognizing the significance of this variation in the context of understanding gas exchange patterns, Buck and Keister (1955) undertook an analysis of variance to demonstrate that most of the variability was among rather than within individuals. This early formal analysis of variance in gas exchange patterns, and later detailed investigations (though with only qualitative analyses) of variability in spiracular movements and vent-ilatory patterns have subsequently largely been overlooked in favour of a focus on the average characteristics of particular gas exchange patterns (Lighton 1998). This focus on the average pattern is also reflected in something of a dissociation between work on the neurophysiology of rhythmic respiratory behaviour and that on gas exchange patterns identified by flow-through respirometry (though see Harrison et al. 1995; Bustami and Hustert 2000). While at first this dissociation might appear surprising, it is, perhaps, understandable given that initial investigations of gas exchange patterns and mechanisms in adult insects were concerned with the extent to which they might also show the discontinuous gas exchange patterns so characteristic of diapausing pupae. Recently, however, attention has once again been drawn to variability in gas exchange patterns, and the reasons for this variability, especially to cast light on the growing debate on the adaptive value of the DGC (Lighton 1998; Chown 2001; Marais and Chown 2003).

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